Apis florea drone flight: longevity and flight performance

Apis florea drone flight: longevity and flight performance
         Ninat Buawangpang, Prachaval Sukumalanand, Michael Burgett

  To cite this version:
 Ninat Buawangpang, Prachaval Sukumalanand, Michael Burgett. Apis florea drone flight:
 longevity and flight performance. Apidologie, Springer Verlag, 2009, 40 (1), pp.20-25. 

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DOI: 10.1051/apido:2008059
                                                                                    Original article

 Apis florea drone flight: longevity and flight performance*

         Ninat Buawangpang1 , Prachaval Sukumalanand1 , Michael Burgett2

      Faculty of Agriculture, Department of Entomology, Chiang Mai University, Chiang Mai, 50200, Thailand
                   Department of Horticulture, Oregon State University, Corvallis, OR 97331, USA

               Received 17 May 2008 – Revised 8 September 2008 – Accepted 30 September 2008

Abstract – Mating flight records are presented for males (drones) of the Asian dwarf honeybee species
Apis florea. These include observations on longevity, mortality and inclusive flight records for a cohort of
known-aged males. Averages for flight performance show the flights/lifetime to be 15.3 (± 11.8 SD); the
number of flight days, 9.1 (± 6.5 SD) and a drone mating flight lasting ca. 31 min (± 9 min, 27 s SD). For
a smaller group of known-aged males, for which complete daily flight performance was recorded for all
days of flight, the mean summed flight time was 6 h 38 min (± 5 h 53 min SD). Longevity and mortality
data show the average age for commencement of flight to be 5.6 days (± 1.3 SD) and the mean age for the
final flight to be 15.6 days (± 9.2 SD), providing an average reproductive flight window of 10 days. These
observations for A. florea male longevity and mortality are significantly shorter than those reported for the
western honeybee (Apis mellifera L.) as observed in temperate climates of North America.

Apis florea / drone / longevity / flight performance

   1. INTRODUCTION                                       cadian flight periods for seven Apis species
                                                         have been examined in any detail (Koeniger
   A recent editorial discussed the paucity of           and Koeniger, 2000; Otis et al., 2000; Rinderer
basic research in the area of honeybee drone             et al., 1993). A good general review of the life
biology and life history (Koeniger, 2005). This          histories of the known Asian honeybee species
reinforces a long-standing neglect in studies of         is to be found in Oldroyd and Wongsiri (2006).
reproductive flight performance and longevity            Somewhat more expansive studies of drone
for male honeybees, most especially for the              flight parameters have been reported for A. flo-
sympatric Asian honeybee species in the genus            rea Fabricius and Apis cerana Fabricius; i.e.,
Apis. As male honeybees contribute to the                average length of reproductive flight, the inter-
overall genetic fitness as much as female re-            flight period in the colony and the daily flight
productives (queens), further studies on male            period (Burgett and Titayavan, 2005; Burgett
honeybees can contribute much to a more                  et al., 2007).
complete understanding of reproductive fit-
ness.                                                       How long male honeybees live and com-
   From a worldwide perspective, longevity               prehensive aspects of their flight performance
and mortality dynamics are best known for                are questions that need addressing for a more
drones of the western honeybee species A.                complete understanding of their reproductive
mellifera L. (Page and Peng, 2001; Rueppell              behavior especially in geographic areas where
et al., 2005). For male reproductive flight dy-          sympatry occurs. Mortality factors for male
namics of Asian Apis species, only the cir-              honeybee reproductive flight include preda-
                                                         tion, mis-orientation, exhaustion (Page and
Corresponding author: M. Burgett,                        Peng, 2001) and the effects of physiological
burgettm@hort.oregonstate.edu                            senescence. Longevity of honeybee males is
* Manuscript editor: Peter Rosenkranz                    best studied in A. mellifera, where numerous

                                   Article published by EDP Sciences
Apis florea drone flight                                          21

reports give average life spans of 20 to 40 days       of drones. Departing drones would most frequently
(Fukuda and Ohtani, 1977; Winston 1987). A             exit the colony from the top portion of the comb.
maximum life span of 59 days was reported by           Returning drones were seen to land anywhere on
Howell and Usinger (1933). We are unaware              the worker bee curtain covering the comb. Observa-
of any comparable longevity studies for drones         tions began in the early afternoons 15 min prior to
of Asian Apis.                                         anticipated drone flight and continued until the fi-
   Apis florea Fabricius, commonly known as            nal return of a marked drone in the mid-afternoon.
the dwarf or small honeybee, is one of two             For the 60 day observational period, drones flew on
                                                       57 days; near the end of the observational period
species of dwarf honeybees found in South-
                                                       in April, traditionally a month with extreme high
east Asia. It builds an exposed single comb
                                                       daytime temperature, three days were character-
nest most frequently in a shaded location              ized by excessive high temperatures (≥ 40 ◦ C) and
(Akratanakul, 1977; Seeley et al., 1982). In           hazy conditions that precluded drone flight from the
northern Thailand during the dry winter sea-           colony. As no apparent differences were seen in any
son, the average A. florea colony occupies a           measured parameter between the two trials, drone
comb area of 490 cm2 , contains 5000 adult             flight data from both trials have been combined.
workers, 35 adult drones, 215 immature drone               Afternoon drone flight was observed daily for
stadia, a single female reproductive and 7 re-         the entire circadian flight period until the disap-
productive queen cells (Burgett and Titayavan,         pearance of the final marked drone(s) at the end
2004).                                                 of the study periods. Drone mortality was assigned
   We report here the results of a study of A.         as the failure of a male to return from a final ob-
florea male flight dynamics and longevity us-          served flight. Individual drone flights were recorded
ing a cohort of known-aged drones as observed          to the h-min-sec Thai standard time (GMT + 7 h).
in northern Thailand during the dry winter pe-         For 20 of the 42 known-aged drones, complete
riod.                                                  flight records were obtained. A complete flight
                                                       record is the observation of all exits and returns
                                                       to the colony until the final disappearance of the
                                                       drone. For the remaining 22 drones, an occasional
   2. METHODS                                          egress or return flight was not observed. However,
                                                       for all 42 drones, data concerning age at first flight,
   All drone flight observations took place on the     age at last flight, total number of flight days and to-
Chiang Mai University campus in northern Thai-         tal number of mating flights were recorded. Flight
land during the months of February, March and          times were corrected to the solar azimuth time ac-
April, 2007, a period when A. florea colonies are      cording to the methodology described by Otis et al.
actively supporting immature and adult drone pop-      (2000).
ulations. To obtain drones of known age, brood
combs possessing pupal drones were incubated
in vitro at 34 ◦ C and a RH of ca. 75%. Emerg-            3. RESULTS
ing drones were harvested at 24 h intervals re-
sulting in a population of 42 known-aged males            3.1. Flight length
which were introduced into an active A. florea
colony that had been transferred to the Chiang Mai         Observed drone flights were separated into
University campus and placed in a shaded envi-         orientation flights lasting < 10 min and mating
ronment ca. 1.5 m above ground suspended be-           flights lasting ≥ 10 min. The average length of
tween two poles. To identify individual drones, the    an A. florea drone mating flight was 31 min
males were marked with numbered, colored tags          4 s (± 9 min 27 s SD, n = 481). The mean
(Opalithplättchen, Chr. Graze KG, Stuttgart, Ger-      flight time for the shorter orientation flights
many). Two trials were conducted over a 60 day         was 4 min 31 s (± 2 min 30 s SD, n = 98).
period. Trial 1, with 13 marked drones, took place
during the period 21 Feb through 11 March and
Trial 2, with 29 marked drones, was conducted dur-        3.2. Circadian flight period
ing the period 12 March through 20 April. To ob-
serve drone flight, two experienced observers vi-        The earliest time a drone commenced flight
sually scanned the comb surface for the presence       was 12:13 (solar azimuth time) and the latest
22                                            N. Buawangpang et al.

Table I. Apis florea vs. A. mellifera drone flight. Total lifetime flights, total days of flight, age at first flight,
and age at last flight. (A. florea data n = 42 |).

                                                       A. florea                       A. mellifera1
              Total lifetime flights             15.3 ± 11.8 {1 – 56}                       ?
              {mean, SD, range}
              Total flight days                    9.1 ± 6.5 {1 – 27}              13.6 ± 9.7 {1 – 38}
              {mean, SD, range}
              Age at 1st flight (days)             5.6 ± 1.3 {3 – 8}               11.1 ± 4.8 {5 – 29}
              {mean, SD, range}
              Age at final flight (days)          15.6 ± 9.2 {6 – 41}             29.9 ± 10.7 {7 – 54}
              {mean, SD, range}
    Data from Rueppell et al., 2005.

return flight was 16:10, a circadian flight pe-                 3.6. Statistical analysis
riod just slightly less than four hours.
                                                                 Standard regression analysis was applied to
                                                             the following variables: (1) drone age at first
     3.3. Drone age at first and last flight                 flight vs. total number of flight days, (2) drone
                                                             age at first flight vs. total number of mating
    The earliest initiation of drone flight was              flights, and (3) drone age at first flight vs. age
3 days old. The oldest age for a drone to inau-              at last flight. For these three conditions no sig-
gurate flight was 8 days. The mean age for first             nificant correlations were shown. High signif-
flight was 5.6 days (± 1.3 SD) and the mean                  icance was shown for the variables total num-
age for final flight was 15.6 days (± 9.2 SD)                ber of flight days vs. total days available for
with a range of 6 to 41 days (Tab. I). This                  flight (R2 = 0.93, P < 0.001) and total life
results in an average reproductive flight win-               time flights vs. total number of flight days
dow of 10 days, following the initiation of first            (R2 = 0.93, P < 0.05).

                                                                4. DISCUSSION
     3.4. Total flight days and total lifetime
          flights                                                When comparing the observations of A. flo-
                                                             rea drones to the temperate A. mellifera model,
                                                             obvious similarities and differences are seen.
   The mean number of flight days was 9.1
                                                             The average A. florea mating flight is some-
(± 6.5 SD), with a range of 1 to 27 days. The
                                                             what longer (by 3 min 28 s) than that reported
average number of total lifetime mating flights
                                                             by Burgett and Titayavan (2005), however the
was 15.3 (± 11.8 SD) with a range of 1 to
                                                             data base we report here is significantly larger
56 flights (Tab. I and Fig. 1).
                                                             than their 2005 report (481 vs. 73 observed
                                                             flights). The length of an average male mating
                                                             flight is comparable for both A. florea and A.
     3.5. Summed flight time                                 mellifera, vin. 30 min (Burgett and Titayavan,
                                                             2005; Howell and Usinger, 1933; Witherell,
   For the cohort of 20 males for which com-                 1972). Comparative observations on A. cerana
plete flight records were obtained, the mean                 drone flight (Burgett et al., 2007) revealed an
summed flight time was 6 h 38 min 20 s (± 5 h                average drone flight time of ca. 16 min which
52 min 51 s SD). This includes both orienta-                 is only about half of the average for A. flo-
tion flights and mating flights (Tab. II).                   rea and A. mellifera. The average A. florea
Apis florea drone flight                                       23

Figure 1. Apis florea drone flight record. Lifespan and flight activity of 42 known-aged drones. Each row
represents a single drone with age (days) on the x-axis coded in gray for no flight activity and black for
flight activity. Drones are sorted according to their lifespan and then age at initiation of flight.

queen mating flight is reported as 18–30 min           Table II. Apis florea drone flight: summed flight
(Koeniger et al., 1989) which corresponds              time for drones with complete flight records and to-
closely to the average A. florea drone flight du-      tal lifetime flights (n = 20 |).
                                                                         Total flight     Total # lifetime
   Our observations on male longevity, age at
                                                                            time              flights
initiation of first flight, and total flight days
                                                        Mean          6 h 38 min 20 s           14.8
are much reduced for A. florea in compari-
                                                        S.D.          5 h 52 min 51 s           11.7
son with those reported for A. mellifera see            Range high    16 h 51 min 19 s           39
(Tab. I). Similar observations for A. cerana are        low            0 h 7 min 37 s            1
not known to exist. Our reported flight win-
dow of ca. 4 h (1213 h to 1610 h) is somewhat
longer than that previously reported (Burgett
and Titayavan, 2005), vin. 1300 h to 1530 h,           29.9 days, while our data for A. florea show
however, in the present study, 98% of all drone        an average lifespan of 15.6 days, with a range
exit flights took place after 13:00 and 93%            of 6 to 41 days. This range breadth for A.
of all return flights occurred before 15:30 h,         florea male longevity (see Fig. 1) displays a
therefore the preponderance of male reproduc-          dramatic intraspecific variation in longevity,
tive flight did occur within a 2.5 h window.           which is comparable to that reported for the
   A comprehensive study of A. mellifera               western honeybee. The average effective re-
drones Rueppell et al. (2005) reported a mean          productive flight window of 10 days for A. flo-
age for initiation of first flight to be 11.1 days;    rea, is slightly more than half of the 18.8 days
this compares to our observation of a mean             given for A. mellifera (Rueppell et al., 2005).
age of 5.6 days for A. florea. They reported              The high correlation for the average num-
a mean lifespan for A. mellifera drones of             ber of A. florea male flight days (9.2), relative
24                                          N. Buawangpang et al.

to the mean flight window of 10 days, demon-             tween the two species is one of a tropically
strates that once a drone commences reproduc-            adapted species relative to a temperate species,
tive flight there is a high probability of con-          each observed in their own respective ecosys-
tinued flight until death. This would support a          tems. It would be illuminating to conduct a
presumed fitness advantage for fast-maturing             comparative study of the temperately adapted
A. florea males as has been postulated for A.            A. mellifera where it has been anthropogeni-
mellifera drones (Rueppell et al., 2005).                cally placed in a tropical ecosystem as exists
    The A. florea data on male flights per life-         in northern Thailand. Further work on addi-
time, age at first flight, age at last flight, the re-   tional Asian Apis species will be of interest in
productive flight window and total time spent            developing a deeper understanding of honey-
in flight are the first to be reported for any           bee drone reproductive behavior for the region
Asian honeybee species. Tables I and II pro-             of the world where Apis species diversity is
vide the statistical summaries. Table I also             at its greatest and where basic research stud-
compares our A. florea observations with those           ies on male behavior have been conspicuously
reported for A. mellifera.                               absent.
    Rueppell et al. (2005) working with A. mel-
lifera, did find a highly significant correlation        Le vol des mâles d’Apis florea : longévité et per-
                                                         formance de vol.
between the age of flight initiation and total
number of days where mating flights were un-             Apis florea / mâle / vol / longévité / performance
dertaken, which is contrary to our findings for
A. florea. The regression analysis for the to-           Zusammenfassung – Der Drohnenflug bei Apis
tal number of A. florea male flights vs. num-            florea: Dauer und Flugleistungen. Bei der westli-
ber of flight days was however, highly signifi-          chen Honigbiene Apis mellifera L. sind die Fluglei-
cant (R2 = 0.93) and this is in agreement with           stungen und das Verhalten beim Drohnenflug sehr
                                                         gut untersucht. Wenig bekannt ist hingegen über das
earlier work on A. mellifera (Witherell, 1972).          Drohnenflugverhalten bei den übrigen 8 Honigbie-
This is an intuitive correlation, i.e., longer           nenarten der Gattung Apis, insbesondere bezüglich
lived males experience more flight days and              der altersabhängigen Flugaktivitäten und der Dau-
hence more reproductive flights in their life-           er der Flüge. Da die Drohnen zu gleichen Teilen
times.                                                   zur genetischen „Fitness“ eines Bienenvolkes bei-
                                                         tragen, sind Untersuchungen zum Paarungssverhal-
    Our data on drone longevity are based on             ten auch für ein besseres Verständnis der Repro-
the assumption that mortality is signified by a          duktionsbiologie wichtig. In Südost-Asien ist dies
drone’s failure to return to its parent colony.          von besonderem Interesse, da hier mehrere Honig-
The causes of the mortality are several and we           bienenarten sympatrisch vorkommen. In dieser Ar-
                                                         beit werden weitere detaillierte Daten zum Droh-
have no way of discriminating between them,              nenflug bei Apis florea F. vorgestellt, einer der zwei
e.g., actual mating with a queen resulting in            Arten von Zwerghonigbienen in Südost-Asien. Die
death; as a victim of any of several predatory           Untersuchungen wurden an der Chiang Mai Univer-
entities; or physiological senescence. Drifting          sität in Nord-Thailand während des Winters 2007
(mis-orientation) to another A. florea colony,           durchgeführt, zu einer Zeit in der viele Drohnen
                                                         in den A. florea-Völkern gepflegt werden. Zur Be-
while not resulting in death, would in our               obachtung des Drohnenfluges wurde ein schwarm-
observations be considered mortality, even               bereites A. florae-Volk auf den Universitätscampus
though those drones who do drift could the-              transportiert. Um altersdefinierte Drohnen zu erhal-
oretically continue future mating flight from            ten, wurde eine Wabe mit schlüpfender Drohnen-
their new location.                                      brut in einem Brutschrank mit 34 ◦ C und 75 % RF
                                                         gehängt und die schlüpfenden Drohnen mit farbigen
    The reproductive life history of A. florea           Nummernplättchen individuell markiert. Diese al-
males can be summarized as relative short                tersdefinierten Drohnen wurden dem A. florae-Volk
and frenetic especially when compared to the             zugegeben. Geschulte Beobachter beobachteten die
only other honeybee species where such ob-               Oberfläche des Bienenvolkes während der nachmit-
servations are known (A. mellifera). Why such            täglichen Flugaktivitäten und erfassten Abflug- und
                                                         Rückkehrzeitpunkt der markierten Drohnen. Die
differences between A. florea and A. mellif-              Beobachtungen wurden so lange fortgeführt, bis der
era drone flight behavior exist is speculative.          letzte altersdefinierte Drohn nicht mehr zum Nest
A comparison of drone flight behavior be-                zurückkehrte.
Apis florea drone flight                                            25

Aus den Flugdaten von 42 Drohnen mit bekanntem           Burgett D.M., Titayavan M. (2005) Apis florea drone
Alter wurden die folgenden Mittelwerte berechnet:            flights: duration, temporal period and inter-flight
Alter beim ersten Flug, Alter beim letzten Flug, An-         period, J. Apic. Res. 44, 36–37.
zahl an Flugtagen, Anzahl der Flüge eines Drohns,
Dauer eines Paarungsfluges und der tägliche Zeit-        Burgett D.M., Titayavan M., Sukumalanand P. (2007)
raum für Drohnenflüge.                                       The drone mating flight of the eastern honeybee
                                                             (Apis cerana F.): duration, temporal period and
Die Aufzeichnungen zu den Drohnenflügen sind in              inter-flight period, Nat. Hist. Bull. Siam Soc. 55,
Abbildung 1 dargestellt. In Tabelle I werden die             99–104.
Mittelwerte für das Alter beim ersten Flug (5,6 Ta-
ge), Alter beim letzten Flug (15,6 Tage), Anzahl         Fukuda H., Ohtani T. (1977) Survival and life span of
Flüge pro Tag (9,1) und die Gesamtzahl an Flügen            drone honey bees, Res. Pop. Ecol. 19, 51–68.
eines Drohns (15,3) zusammengefasst. In Tabelle I
werden diese Parameter zusätzlich mit bekannten          Howell D.E., Usinger R.L. (1933) Observations on
Daten von A. mellifera-Drohnen verglichen. Der              the flight and length of life of drone bees, Ann.
durchschnittliche Paarungsflug von A. florea dauert         Entomol. Soc. Am. 26, 239–246.
31 Min. und findet während eines Zeitraumes statt,       Koeniger G. (2005) The neglected gender – males in
der um ca. 12,00 beginnt und um ca. 14,00 endet.            bees, Apidologie 36, 143–144.
Von einer Gruppe von 20 altersdefinierten Drohnen,
für die vollständige Aufzeichnungen vom ersten bis       Koeniger N., Koeniger G. (2000) Reproductive isola-
zum letzten Flug vorlagen, wurde eine mittlere Ge-          tion among species of the genus Apis, Apidologie
samtflugzeit von 6h und 38 Min. berechnet, wo-              31, 313–339.
bei es erhebliche Schwankungen gab. Die maximale
Flugzeit für einen Drohn betrug 16 h und 51 Min.,        Koeniger N., Koeniger G., Wongsiri S. (1989) Mating
verteilt auf 39 Flüge an 25 Flugtagen.                      and sperm transfer in Apis florae, Apidologie 21,
Da bisher wenig über die Flugleistungen bei den
Drohnen der übrigen 7 asiatischen Apis-Arten be-         Oldroyd B.P., Wongsiri S. (2006) Asian Honey Bees:
kannt ist, verglichen wir unsere Beobachtungen an            Biology, Conservation and Human Resources,
Drohnen von A. florea als eine an die Tropen ange-           Harvard Univ. Press, Cambridge, MA.
passte Bienenart mit den Drohnen einer an gemä-
ßigte Klimate angepassten Art (A. mellifera).            Otis G.W., Koeniger N., Rinderer T.E., Hadisoesilo S.,
Auffällig ist zunächst die Ähnlichkeit bei der Länge          Yoshida T., Tingek S., Wongsiri S., Mardan M.B.
des Paarungsfluges (ca. 30 Min. für beide Arten).            (2000) Comparative mating flight times of Asian
Für die Anzahl an Flugtagen, das Alter beim ersten           honey bees, Proc. 7th Int. Conf. on Tropical Bee
                                                             Management and Diversity and 5th Asian Apic.
Flug sowie das Alter beim letzten Flug wurden für            Assoc. Conf. 19–25 March 2000, Chiang Mai,
die Drohnen von A. florea dagegen deutlich gerin-            Thailand, IBRA, Cardiff, UK, pp. 137–141.
gere Werte festgestellt. Im Vergleich zu A. melli-
fera kann die Flugaktivität von A. florea-Drohnen        Page R.E., Peng C.Y.-S. (2001) Aging and develop-
daher als „kurz und heftig“ zusammengefasst wer-             ment in social insects with emphasis on the honey
den. Sinnvoller wäre allerdings ein Vergleich mit            bee Apis mellifera L, Exp. Gerontol. 36, 695–711.
der Drohnenflugcharakteristik von anderen sympa-
trischen Apis Arten in Südost-Asien; allerdings wä-      Rinderer T.E., Oldroyd B.P., Wongsiri S., Sylvester
ren hierfür mehr Forschungen an diesen Bienenar-             H.A., Guzman L.I., Potichot S., Sheppard W.S.
ten notwendig.                                               et al. (1993) Time of drone flight in four honey bee
                                                             species in south-eastern Thailand, J. Apic. Res. 32,
Apis florea / Drohnen / Dauer / Flugleistung                 27–33.
                                                         Rueppell O., Fondrk M.K., Page R.E. (2005)
                                                            Biodemographic analysis of male honey bee mor-
                                                            tality, Aging Cell 4, 13–19.
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